Gastroenteropancreatic neuroendocrine neoplasms: Historical context and current issues

Seminars in Diagnostic Pathology

Volumn 30, Issue 3, 2013, Pages 186-196

  Yang, Zhaohai ^a   Tang, Laura H ^b   Klimstra, David S ^b  

^a PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Carcinoid tumor; Ki67 antigen; Neoplasm grading; Neoplasm staging; Neuroendocrine tumors; Pancreatic neoplasms

Indexed keywords

CHROMOGRANIN A; KI 67 ANTIGEN; SYNAPTOPHYSIN; VESICULAR MONOAMINE TRANSPORTER 2;

ARTICLE; CANCER GRADING; CANCER PROGNOSIS; CANCER STAGING; CELLULAR DISTRIBUTION; DIGITAL IMAGING; GASTROENTEROPANCREATIC NEUROENDOCRINE TUMOR; HISTOPATHOLOGY; HISTORY OF MEDICINE; HUMAN; IMAGE ANALYSIS; MITOSIS RATE; NEUROSECRETORY CELL; NOMENCLATURE; POORLY DIFFERENTIATED NEUROENDOCRINE CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REFERENCE VALUE; STANDARDIZATION; TUMOR INVASION; TUMOR NECROSIS; TUMOR VOLUME;

CARCINOID TUMOR; KI67 ANTIGEN; NEOPLASM GRADING; NEOPLASM STAGING; NEUROENDOCRINE TUMORS; PANCREATIC NEOPLASMS;

HUMANS; INTESTINAL NEOPLASMS; NEUROENDOCRINE TUMORS; PANCREATIC NEOPLASMS; STOMACH NEOPLASMS;

EID: 84885944934     PISSN: 07402570     EISSN: 19301111     Source Type: Journal    
DOI: 10.1053/j.semdp.2013.06.005     Document Type: Article

References (63)

1. Lawrence B., Gustafsson B.I., Chan A., Svejda B., Kidd M., Modlin I.M. The epidemiology of gastroenteropancreatic neuroendocrine tumors. Endocrinol Metab Clin North Am 2011, 40:1-18. vii.
2. Moertel C.G. Karnofsky memorial lecture. An odyssey in the land of small tumors. J Clin Oncol 1987, 5:1502-1522.
3. Rosai J. The origin of neuroendocrine tumors and the neural crest saga. Mod Pathol 2011, 24(suppl 2):S53-S57.
4. Pearse A.G., Polak J.M. Neural crest origin of the endocrine polypeptide (APUD) cells of the gastrointestinal tract and pancreas. Gut 1971, 12:783-788.
5. Cheng H., Leblond C.P. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. III. Entero-endocrine cells. Am J Anat 1974, 141:503-519.
6. Fontaine J., Le Douarin N.M. Analysis of endoderm formation in the avian blastoderm by the use of quail-chick chimaeras. The problem of the neurectodermal origin of the cells of the APUD series. J Embryol Exp Morphol 1977, 41:209-222.
7. Flemstrom G., Sjoblom M. Epithelial cells and their neighbors. II. New perspectives on efferent signaling between brain, neuroendocrine cells, and gut epithelial cells. Am J Physiol Gastrointest Liver Physiol 2005, 289:G377-G380.
8. Capella C., Heitz P.U., Hofler H., Solcia E., Kloppel G. Revised classification of neuroendocrine tumours of the lung, pancreas and gut. Virchows Arch 1995, 425:547-560.
9. Bordi C., D'Adda T., Azzoni C., Ferraro G. Classification of gastric endocrine cells at the light and electron microscopical levels. Microsc Res Tech 2000, 48:258-271.
10. Sundler F., Eriksson B., Grimelius L., Hakanson R., Lonroth H., Lundell L. Histamine in gastric carcinoid tumors: immunocytochemical evidence. Endocr Pathol 1992, 3:23-27.
11. Eissele R., Anlauf M., Schafer M.K., Eiden L.E., Arnold R., Weihe E. Expression of vesicular monoamine transporters in endocrine hyperplasia and endocrine tumors of the oxyntic stomach. Digestion 1999, 60:428-439.
12. Tang L.H., Song L., Shia J.R., Klimstra D.S. Identification of histidine decarboxylase (HDC) positive endocrine cells in subtypes of gastric carcinoid tumors using highly sensitive and specific chromogen in situ hybridization (CISH). Mod Pathol 2006, 19:121A. [Abstract #552].
13. Poynter D., Selway S.A. Neuroendocrine cell hyperplasia and neuroendocrine carcinoma of the rodent fundic stomach. Mutat Res 1991, 248:303-319.
14. Solcia E., Bordi C., Creutzfeldt W., Dayal Y., Dayan A.D., Falkmer S., et al. Histopathological classification of nonantral gastric endocrine growths in man. Digestion 1988, 41:185-200.
15. Sjolund K., Sanden G., Hakanson R., Sundler F. Endocrine cells in human intestine: an immunocytochemical study. Gastroenterology 1983, 85:1120-1130.
16. Hruban R.H., Pitman M.B., Klimstra D.S. The normal pancreas. Tumors of the Pancreas 2007, 1-22. ARP/AFIP, Washington, DC. R.H. Hruban, M.B. Pitman, D.S. Klimstra (Eds.).
17. Kloppel G. Oberndorfer and his successors: from carcinoid to neuroendocrine carcinoma. Endocr Pathol 2007, 18:141-144.
18. Kloppel G., Perren A., Heitz P.U. The gastroenteropancreatic neuroendocrine cell system and its tumors: the WHO classification. Ann N Y Acad Sci 2004, 1014:13-27.
19. Capella C., Solcia E., Sobin L.H., Arnold R. Endocrine tumours of the stomach. WHO Classification of Tumours. Pathology & Genetics of Tumours of the Digestive System 2000, 53-57. IARC Press, Lyon. S.R. Hamilton, L.A. Aaltonen (Eds.).
20. Heitz P.U., Komminoth P., Perren A., Klimstra D.S., Dayal Y., Bordi C., et al. Pancreatic endocrine tumours: Introduction. Pathology and Genetics of Tumours of Endocrine Organs 2004, 177-182. IARC Press, Lyon. R.A. DeLellis, R.V. Lloyd, P.U. Heitz (Eds.).
21. WHO Classification of Tumours of the Digestive System 2010, IARC Press, Lyon, France. F. Bosman, F. Carneiro, R. Hruban, N. Theise (Eds.).
22. Travis W.D. The concept of pulmonary neuroendocrine tumours. Pathology and Genetics of Tumours of the Lung, Pleura, Thymus and Heart 2004, 19-20. IARC Press, Lyon, France. W.D. Travis, E. Brambilla, H.K. Muller-Hermelink (Eds.).
23. Williams E.D., Sandler M. The classification of carcinoid tumours. Lancet 1963, 1:238-239.
24. Soga J., Tazawa K. Pathologic analysis of carcinoids. Histologic reevaluation of 62 cases. Cancer 1971, 28:990-998.
25. Ekeblad S., Skogseid B., Dunder K., Oberg K., Eriksson B. Prognostic factors and survival in 324 patients with pancreatic endocrine tumor treated at a single institution. Clin Cancer Res 2008, 14:7798-7803.
26. Ferrone C.R., Tang L.H., Tomlinson J., Gonen M., Hochwald S.N., Brennan M.F., et al. Determining prognosis in patients with pancreatic endocrine neoplasms: can the WHO classification system be simplified?. J Clin Oncol 2007, 25:5609-5615.
27. Formica V, Wotherspoon A., Cunningham D., Norman A.R., Sirohi B., Oates J., et al. The prognostic role of WHO classification, urinary 5-hydroxyindoleacetic acid and liver function tests in metastatic neuroendocrine carcinomas of the gastroenteropancreatic tract. Br J Cancer 2007, 96:1178-1182.
28. Schindl M., Kaczirek K., Kaserer K., Niederle B. Is the new classification of neuroendocrine pancreatic tumors of clinical help?. World J Surg 2000, 24:1312-1318.
29. Rindi G., Kloppel G., Alhman H., Caplin M., Couvelard A., de Herder W.W., et al. TNM staging of foregut (neuro) endocrine tumors: a consensus proposal including a grading system. Virchows Arch 2006, 449:395-401.
30. Rindi G., Kloppel G., Couvelard A., Komminoth P., Korner M., Lopes J.M., et al. TNM staging of midgut and hindgut (neuro) endocrine tumors: a consensus proposal including a grading system. Virchows Arch 2007, 451:757-762.
31. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A. eds, AJCC Cancer Staging Manual. New York: Springer; 2010, p. 648.
32. Travis W.D., Rush W., Flieder D.B., Falk R., Fleming M.V., Gal A.A., et al. Survival analysis of 200 pulmonary neuroendocrine tumors with clarification of criteria for atypical carcinoid and its separation from typical carcinoid. Am J Surg Pathol 1998, 22:934-944.
33. Moran C.A., Suster S. Neuroendocrine carcinomas (carcinoid tumor) of the thymus. A clinicopathologic analysis of 80 cases. Am J Clin Pathol 2000, 114:100-110.
34. La Rosa S., Sessa F., Capella C., Riva C., Leone B.E., Klersy C., et al. Prognostic criteria in nonfunctioning pancreatic endocrine tumours. Virchows Arch 1996, 429:323-333.
35. La Rosa S., Klersy C., Uccella S., Dainese L., Albarello L., Sonzogni A., et al. Improved histologic and clinicopathologic criteria for prognostic evaluation of pancreatic endocrine tumors. Hum Pathol 2009, 40:30-40.
36. Ohike N., Morohoshi T. Pathological assessment of pancreatic endocrine tumors for metastatic potential and clinical prognosis. Endocr Pathol 2005, 16:33-40.
37. Pelosi G., Bresaola E., Bogina G., Pasini F., Rodella S., Castelli P., et al. Endocrine tumors of the pancreas: Ki-67 immunoreactivity on paraffin sections is an independent predictor for malignancy: a comparative study with proliferating-cell nuclear antigen and progesterone receptor protein immunostaining, mitotic index, and other clinicopathologic variables. Hum Pathol 1996, 27:1124-1134.
38. Khan M.S., Luong T.V., Watkins J., Toumpanakis C., Caplin M.E., Meyer T. A comparison of Ki-67 and mitotic count as prognostic markers for metastatic pancreatic and midgut neuroendocrine neoplasms. Br J Cancer 2013, 108:1838-1845.
39. Cho C.S., Labow D.M., Tang L., Klimstra D.S., Loeffler A.G., Leverson G.E., et al. Histologic grade is correlated with outcome after resection of hepatic neuroendocrine neoplasms. Cancer 2008, 113:126-134.
40. Hochwald S.N., Zee S., Conlon K.C., Colleoni R., Louie O., Brennan M.F., et al. Prognostic factors in pancreatic endocrine neoplasms: an analysis of 136 cases with a proposal for low-grade and intermediate-grade groups. J Clin Oncol 2002, 20:2633-2642.
41. Hamilton SR, Aaltonen LA eds. World Health Organization Classification of Tumours: Pathology and Genetics of Tumours of the Digestive System. Lyon: IARC Press; 2000, p. 314.
42. Jann H., Roll S., Couvelard A., Hentic O., Pavel M., Muller-Nordhorn J., et al. Neuroendocrine tumors of midgut and hindgut origin: tumor-node-metastasis classification determines clinical outcome. Cancer 2011, 117:3332-3341.
43. La Rosa S., Inzani F., Vanoli A., Klersy C., Dainese L., Rindi G., et al. Histologic characterization and improved prognostic evaluation of 209 gastric neuroendocrine neoplasms. Hum Pathol 2011.
44. Pape U.F., Jann H., Muller-Nordhorn J., Bockelbrink A., Berndt U., Willich S.N., et al. Prognostic relevance of a novel TNM classification system for upper gastroenteropancreatic neuroendocrine tumors. Cancer 2008, 113:256-265.
45. Strosberg J., Nasir A., Coppola D., Wick M., Kvols L. Correlation between grade and prognosis in metastatic gastroenteropancreatic neuroendocrine tumors. Hum Pathol 2009, 40:1262-1268.
46. Yang Z., Tang L.H., Klimstra D.S. Effect of tumor heterogeneity on the assessment of Ki67 labeling index in well-differentiated neuroendocrine tumors metastatic to the liver: implications for prognostic stratification. Am J Surg Pathol 2011, 35:853-860.
47. Panzuto F., Boninsegna L., Fazio N., Campana D., Pia Brizzi M., Capurso G., et al. Metastatic and locally advanced pancreatic endocrine carcinomas: analysis of factors associated with disease progression. J Clin Oncol 2011, 29:2372-2377.
48. Klimstra D.S., Modlin I.R., Adsay N.V., Chetty R., Deshpande V., Gonen M., et al. Pathology reporting of neuroendocrine tumors: application of the Delphic consensus process to the development of a minimum pathology data set. Am J Surg Pathol 2010, 34:300-313.
49. Klimstra DS, Yang Z. Pathology, classifica tion, and grading of neuroendocrine tumors arising in the digestive system. In: Goldberg RM, Savarese DF eds. UpToDate. edn, Vol, UpToDate: Waltham, MA, 2013.
50. Tang L.H., Gonen M., Hedvat C., Modlin I.M., Klimstra D.S. Objective quantification of the Ki67 proliferative index in neuroendocrine tumors of the gastroenteropancreatic system: a comparison of digital image analysis with manual methods. Am J Surg Pathol 2012, 36:1761-1770.
51. McCall C.M., Shi C., Ellison T., Hruban R.H., Wolfgang C., Schulick R., et al. Ki-67 proliferation index and mitotic rate discordance in pancreatic neuroendocrine tumors correlates with aggressive histologic features and decreased overall survival. Mod Pathol 2012, 25:446A-447A. [Abstract #1863].
52. Basturk O., Yang Z., Tang L.H., Hruban R., McCall C., Adsay V., et al. Increased (>20%) Ki67 proliferation index in morphologically well differentiated pancreatic neuroendocrine tumors (PanNETs) correlates with decreased overall survival. Mod Pathol 2013, 26:463A. [Abstract #1761].
53. Sorbye H., Welin S., Langer S.W., Vestermark L.W., Holt N., Osterlund P., et al. Predictive and prognostic factors for treatment and survival in 305 patients with advanced gastrointestinal neuroendocrine carcinoma (WHO G3): the NORDIC NEC study. Ann Oncol 2013, 24:152-160.
54. Couvelard A., Deschamps L., Ravaud P., Baron G., Sauvanet A., Hentic O., et al. Heterogeneity of tumor prognostic markers: a reproducibility study applied to liver metastases of pancreatic endocrine tumors. Mod Pathol 2009, 22:273-281.
55. Goh B.K., Chow P.K., Tan Y.M., Cheow P.C., Chung Y.F., Soo K.C., et al. Validation of five contemporary prognostication systems for primary pancreatic endocrine neoplasms: results from a single institution experience with 61 surgically treated cases. ANZ J Surg 2011, 81:79-85.
56. Scarpa A., Mantovani W., Capelli P., Beghelli S., Boninsegna L., Bettini R., et al. Pancreatic endocrine tumors: improved TNM staging and histopathological grading permit a clinically efficient prognostic stratification of patients. Mod Pathol 2010, 23:824-833.
57. Strosberg J.R., Cheema A., Weber J., Han G., Coppola D., Kvols L.K. Prognostic validity of a novel American Joint Committee on Cancer Staging Classification for pancreatic neuroendocrine tumors. J Clin Oncol 2011, 29:3044-3049.
58. Dolcetta-Capuzzo A., Villa V., Albarello L., Franchi G.M., Gemma M., Scavini M., et al. Gastroenteric neuroendocrine neoplasms classification: comparison of prognostic models. Cancer 2013, 119:36-44.
59. Rindi G., Falconi M., Klersy C., Albarello L., Boninsegna L., Buchler M.W., et al. TNM staging of neoplasms of the endocrine pancreas: results from a large international cohort study. J Natl Cancer Inst 2012, 104:764-777.
60. Brenner B., Tang L.H., Klimstra D.S., Kelsen D.P. Small-cell carcinomas of the gastrointestinal tract: a review. J Clin Oncol 2004, 22:2730-2739.
61. Shia J., Tang L.H., Weiser M.R., Brenner B., Adsay N.V., Stelow E.B., et al. Is nonsmall cell type high-grade neuroendocrine carcinoma of the tubular gastrointestinal tract a distinct disease entity?. Am J Surg Pathol 2008, 32:719-731.
62. Kulke MH, Benson AB 3rd, Bergsland E, Berlin JD, Blaszkowsky LS, Choti MA, et al. NCCN clinical practice guidelines in oncology: Neuroendocrine tumors. edn, Vol. V.2.2013. National Comprehensive Cancer Network. 2013.
63. Tang L., Shia J., Vakiani E., Dhall D., Klimstra D.S. High grade transformation of differentiated neuroendocrine neoplasms (NENs) of the enteropancreatic system-a unique entity distinct from de novo high grade neuroendocrine carcinoma (HGNECa) in pathogenesis and clinical behavior. Mod Pathol 2008, 21:137A. [Abstract #622].